{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T13:05:52Z","timestamp":1791291952747,"version":"4.1.0"},"reference-count":38,"publisher":"National Academy of Sciences","issue":"26","content-domain":{"domain":["www.pnas.org"],"crossmark-restriction":true},"short-container-title":["Proc. Natl. Acad. Sci. U.S.A."],"published-print":{"date-parts":[[2010,6,29]]},"abstract":"<jats:p>\n                    Rift Valley fever virus (RVFV) is a negative-sense RNA virus (genus\n                    <jats:italic>Phlebovirus<\/jats:italic>\n                    , family\n                    <jats:italic>Bunyaviridae<\/jats:italic>\n                    ) that infects livestock and humans and is endemic to sub-Saharan Africa. Like all negative-sense viruses, the segmented RNA genome of RVFV is encapsidated by a nucleocapsid protein (N). The 1.93-\u212b crystal structure of RVFV N and electron micrographs of ribonucleoprotein (RNP) reveal an encapsidated genome of substantially different organization than in other negative-sense RNA virus families. The RNP polymer, viewed in electron micrographs of both virus RNP and RNP reconstituted from purified N with a defined RNA, has an extended structure without helical symmetry. N-RNA species of \u223c100-kDa apparent molecular weight and heterogeneous composition were obtained by exhaustive ribonuclease treatment of virus RNP, by recombinant expression of N, and by reconstitution from purified N and an RNA oligomer. RNA-free N, obtained by denaturation and refolding, has a novel all-helical fold that is compact and well ordered at both the N and C termini. Unlike N of other negative-sense RNA viruses, RVFV N has no positively charged surface cleft for RNA binding and no protruding termini or loops to stabilize a defined N-RNA oligomer or RNP helix. A potential protein interaction site was identified in a conserved hydrophobic pocket. The nonhelical appearance of phlebovirus RNP, the heterogeneous \u223c100-kDa N-RNA multimer, and the N fold differ substantially from the RNP and N of other negative-sense RNA virus families and provide valuable insights into the structure of the encapsidated phlebovirus genome.\n                  <\/jats:p>","DOI":"10.1073\/pnas.1001760107","type":"journal-article","created":{"date-parts":[[2010,6,15]],"date-time":"2010-06-15T00:19:00Z","timestamp":1276561140000},"page":"11769-11774","update-policy":"https:\/\/doi.org\/10.1073\/pnas.cm10313","source":"Crossref","is-referenced-by-count":130,"title":["Structure of the Rift Valley fever virus nucleocapsid protein reveals another architecture for RNA encapsidation"],"prefix":"10.1073","volume":"107","author":[{"given":"Donald D.","family":"Raymond","sequence":"first","affiliation":[{"name":"Life Sciences Institute,"},{"name":"Department of Biological Chemistry,"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mary E.","family":"Piper","sequence":"additional","affiliation":[{"name":"Cellular and Molecular Biology Program, and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sonja R.","family":"Gerrard","sequence":"additional","affiliation":[{"name":"Cellular and Molecular Biology Program, and"},{"name":"Department of Epidemiology, University of Michigan, Ann Arbor, MI 48109"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Janet L.","family":"Smith","sequence":"additional","affiliation":[{"name":"Life Sciences Institute,"},{"name":"Department of Biological Chemistry,"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"341","published-online":{"date-parts":[[2010,6,14]]},"reference":[{"key":"e_1_3_4_1_2","first-page":"83","volume-title":"Principles of virology : Molecular biology, pathogenesis, and control of animal viruses","author":"Flint SJ","year":"2004","unstructured":"SJ Flint, LW Enquist, VR Racaniello, AM Skalka Principles of virology : Molecular biology, pathogenesis, and control of animal viruses (ASM Press, Washington), pp. 83\u2013125 (2004)."},{"key":"e_1_3_4_2_2","first-page":"1603","volume-title":"Fields Virology","author":"Nichol ST","year":"2001","unstructured":"ST Nichol Fields Virology, eds BN Fields, DM Knipe, PM Howley, DE Griffin (Lippincott, Williams & Wilkins, Philadelphia), pp. 1603\u20131633 (2001)."},{"key":"e_1_3_4_3_2","first-page":"1581","volume-title":"Fields Virology","author":"Schmaljohn CS","year":"2001","unstructured":"CS Schmaljohn, JW Hooper Fields Virology, eds BN Fields, DM Knipe, PM Howley, DE Griffin (Lippincott, Williams & Wilkins, Philadelphia), pp. 1581\u20131602 (2001)."},{"key":"e_1_3_4_4_2","first-page":"1741","volume-title":"Fields Virology","author":"Schmaljohn CS","year":"2007","unstructured":"CS Schmaljohn, ST Nichol Fields Virology, eds DM Knipe, et al. (Lippincott, Williams & Wilkins, Philadelphia), pp. 1741\u20131789 (2007)."},{"key":"e_1_3_4_5_2","doi-asserted-by":"crossref","first-page":"3198","DOI":"10.1128\/JVI.02655-06","article-title":"The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging","volume":"81","author":"Overby AK","year":"2007","unstructured":"AK Overby, RF Pettersson, EP Neve, The glycoprotein cytoplasmic tail of Uukuniemi virus (Bunyaviridae) interacts with ribonucleoproteins and is critical for genome packaging. J Virol 81, 3198\u20133205 (2007).","journal-title":"J Virol"},{"key":"e_1_3_4_6_2","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1261\/rna.1367209","article-title":"Investigating the specificity and stoichiometry of RNA binding by the nucleocapsid protein of Bunyamwera virus","volume":"15","author":"Mohl BP","year":"2009","unstructured":"BP Mohl, JN Barr, Investigating the specificity and stoichiometry of RNA binding by the nucleocapsid protein of Bunyamwera virus. RNA 15, 391\u2013399 (2009).","journal-title":"RNA"},{"key":"e_1_3_4_7_2","doi-asserted-by":"crossref","first-page":"332","DOI":"10.1006\/viro.1993.1263","article-title":"RNA binding of recombinant nucleocapsid proteins of hantaviruses","volume":"194","author":"Gott P","year":"1993","unstructured":"P Gott, R Stohwasser, P Schnitzler, G Darai, EK Bautz, RNA binding of recombinant nucleocapsid proteins of hantaviruses. Virology 194, 332\u2013337 (1993).","journal-title":"Virology"},{"key":"e_1_3_4_8_2","doi-asserted-by":"crossref","first-page":"9946","DOI":"10.1128\/JVI.74.21.9946-9952.2000","article-title":"RNA binding properties of bunyamwera virus nucleocapsid protein and selective binding to an element in the 5\u2032 terminus of the negative-sense S segment","volume":"74","author":"Osborne JC","year":"2000","unstructured":"JC Osborne, RM Elliott, RNA binding properties of bunyamwera virus nucleocapsid protein and selective binding to an element in the 5\u2032 terminus of the negative-sense S segment. J Virol 74, 9946\u20139952 (2000).","journal-title":"J Virol"},{"key":"e_1_3_4_9_2","doi-asserted-by":"crossref","first-page":"11283","DOI":"10.1128\/JVI.00820-06","article-title":"Hantavirus N protein exhibits genus-specific recognition of the viral RNA panhandle","volume":"80","author":"Mir MA","year":"2006","unstructured":"MA Mir, B Brown, B Hjelle, WA Duran, AT Panganiban, Hantavirus N protein exhibits genus-specific recognition of the viral RNA panhandle. J Virol 80, 11283\u201311292 (2006).","journal-title":"J Virol"},{"key":"e_1_3_4_10_2","doi-asserted-by":"crossref","first-page":"13754","DOI":"10.1128\/JVI.01492-07","article-title":"RNA binding domain of Jamestown Canyon virus S segment RNAs","volume":"81","author":"Ogg MM","year":"2007","unstructured":"MM Ogg, JL Patterson, RNA binding domain of Jamestown Canyon virus S segment RNAs. J Virol 81, 13754\u201313760 (2007).","journal-title":"J Virol"},{"key":"e_1_3_4_11_2","doi-asserted-by":"crossref","first-page":"33732","DOI":"10.1074\/jbc.274.47.33732","article-title":"Characterization of the Hantaan nucleocapsid protein-ribonucleic acid interaction","volume":"274","author":"Severson W","year":"1999","unstructured":"W Severson, L Partin, CS Schmaljohn, CB Jonsson, Characterization of the Hantaan nucleocapsid protein-ribonucleic acid interaction. J Biol Chem 274, 33732\u201333739 (1999).","journal-title":"J Biol Chem"},{"key":"e_1_3_4_12_2","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1146\/annurev.phyto.36.1.139","article-title":"Biology and molecular biology of viruses in the genus Tenuivirus","volume":"36","author":"Falk BW","year":"1998","unstructured":"BW Falk, JH Tsai, Biology and molecular biology of viruses in the genus Tenuivirus. Annu Rev Phytopathol 36, 139\u2013163 (1998).","journal-title":"Annu Rev Phytopathol"},{"key":"e_1_3_4_13_2","doi-asserted-by":"crossref","first-page":"1078","DOI":"10.1038\/nature05379","article-title":"The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA","volume":"444","author":"Ye Q","year":"2006","unstructured":"Q Ye, RM Krug, YJ Tao, The mechanism by which influenza A virus nucleoprotein forms oligomers and binds RNA. Nature 444, 1078\u20131082 (2006).","journal-title":"Nature"},{"key":"e_1_3_4_14_2","doi-asserted-by":"crossref","first-page":"360","DOI":"10.1126\/science.1125280","article-title":"Crystal structure of the rabies virus nucleoprotein-RNA complex","volume":"313","author":"Albertini AA","year":"2006","unstructured":"AA Albertini, et al., Crystal structure of the rabies virus nucleoprotein-RNA complex. Science 313, 360\u2013363 (2006).","journal-title":"Science"},{"key":"e_1_3_4_15_2","doi-asserted-by":"crossref","first-page":"1279","DOI":"10.1126\/science.1177634","article-title":"Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus","volume":"326","author":"Tawar RG","year":"2009","unstructured":"RG Tawar, et al., Crystal structure of a nucleocapsid-like nucleoprotein-RNA complex of respiratory syncytial virus. Science 326, 1279\u20131283 (2009).","journal-title":"Science"},{"key":"e_1_3_4_16_2","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1126\/science.1126953","article-title":"Structure of the vesicular stomatitis virus nucleoprotein-RNA complex","volume":"313","author":"Green TJ","year":"2006","unstructured":"TJ Green, X Zhang, GW Wertz, M Luo, Structure of the vesicular stomatitis virus nucleoprotein-RNA complex. Science 313, 357\u2013360 (2006).","journal-title":"Science"},{"key":"e_1_3_4_17_2","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1016\/j.str.2003.08.011","article-title":"Crystal structure of the borna disease virus nucleoprotein","volume":"11","author":"Rudolph MG","year":"2003","unstructured":"MG Rudolph, et al., Crystal structure of the borna disease virus nucleoprotein. Structure 11, 1219\u20131226 (2003).","journal-title":"Structure"},{"key":"e_1_3_4_18_2","doi-asserted-by":"crossref","first-page":"e1000491","DOI":"10.1371\/journal.ppat.1000491","article-title":"The structure of a biologically active influenza virus ribonucleoprotein complex","volume":"5","author":"Coloma R","year":"2009","unstructured":"R Coloma, et al., The structure of a biologically active influenza virus ribonucleoprotein complex. PLoS Pathog 5, e1000491 (2009).","journal-title":"PLoS Pathog"},{"key":"e_1_3_4_19_2","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/0042-6822(69)90057-9","article-title":"The inner structure of Uukuniemi and two Bunyamwera supergroup arboviruses","volume":"39","author":"von Bonsdorff CH","year":"1969","unstructured":"CH von Bonsdorff, P Saikku, N Oker-Blom, The inner structure of Uukuniemi and two Bunyamwera supergroup arboviruses. Virology 39, 342\u2013344 (1969).","journal-title":"Virology"},{"key":"e_1_3_4_20_2","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1128\/jvi.15.2.386-392.1975","article-title":"Ribonucleoproteins of Uukuniemi virus are circular","volume":"15","author":"Pettersson RF","year":"1975","unstructured":"RF Pettersson, CH von Bonsdorff, Ribonucleoproteins of Uukuniemi virus are circular. J Virol 15, 386\u2013392 (1975).","journal-title":"J Virol"},{"key":"e_1_3_4_21_2","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.jmb.2004.03.073","article-title":"The 12\u00a0A structure of trypsin-treated measles virus N-RNA","volume":"339","author":"Schoehn G","year":"2004","unstructured":"G Schoehn, et al., The 12\u00a0A structure of trypsin-treated measles virus N-RNA. J Mol Biol 339, 301\u2013312 (2004).","journal-title":"J Mol Biol"},{"key":"e_1_3_4_22_2","doi-asserted-by":"crossref","first-page":"1831","DOI":"10.1099\/0022-1317-83-8-1831","article-title":"Significant differences in nucleocapsid morphology within the Paramyxoviridae","volume":"83","author":"Bhella D","year":"2002","unstructured":"D Bhella, A Ralph, LB Murphy, RP Yeo, Significant differences in nucleocapsid morphology within the Paramyxoviridae. J Gen Virol 83, 1831\u20131839 (2002).","journal-title":"J Gen Virol"},{"key":"e_1_3_4_23_2","doi-asserted-by":"crossref","first-page":"689","DOI":"10.1126\/science.1181766","article-title":"Cryo-EM model of the bullet-shaped vesicular stomatitis virus","volume":"327","author":"Ge P","year":"2010","unstructured":"P Ge, et al., Cryo-EM model of the bullet-shaped vesicular stomatitis virus. Science 327, 689\u2013693 (2010).","journal-title":"Science"},{"key":"e_1_3_4_24_2","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.1099\/0022-1317-76-4-1009","article-title":"Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles","volume":"76","author":"Ruigrok RW","year":"1995","unstructured":"RW Ruigrok, F Baudin, Structure of influenza virus ribonucleoprotein particles. II. Purified RNA-free influenza virus ribonucleoprotein forms structures that are indistinguishable from the intact influenza virus ribonucleoprotein particles. J Gen Virol 76, 1009\u20131014 (1995).","journal-title":"J Gen Virol"},{"key":"e_1_3_4_25_2","doi-asserted-by":"crossref","first-page":"11974","DOI":"10.1128\/JVI.79.18.11974-11980.2005","article-title":"The N terminus of Rift Valley fever virus nucleoprotein is essential for dimerization","volume":"79","author":"Le May N","year":"2005","unstructured":"N Le May, N Gauliard, A Billecocq, M Bouloy, The N terminus of Rift Valley fever virus nucleoprotein is essential for dimerization. J Virol 79, 11974\u201311980 (2005).","journal-title":"J Virol"},{"key":"e_1_3_4_26_2","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/S0968-0004(00)89105-7","article-title":"Dali: A network tool for protein structure comparison","volume":"20","author":"Holm L","year":"1995","unstructured":"L Holm, C Sander, Dali: A network tool for protein structure comparison. Trends Biochem Sci 20, 478\u2013480 (1995).","journal-title":"Trends Biochem Sci"},{"key":"e_1_3_4_27_2","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/S0959-440X(96)80058-3","article-title":"Surprising similarities in structure comparison","volume":"6","author":"Gibrat JF","year":"1996","unstructured":"JF Gibrat, T Madej, SH Bryant, Surprising similarities in structure comparison. Curr Opin Struct Biol 6, 377\u2013385 (1996).","journal-title":"Curr Opin Struct Biol"},{"key":"e_1_3_4_28_2","doi-asserted-by":"crossref","first-page":"731","DOI":"10.3390\/v2030731","article-title":"A novel system for identification of inhibitors of Rift Valley fever virus replication","volume":"2","author":"Piper M","year":"2010","unstructured":"M Piper, S Gerrard, A novel system for identification of inhibitors of Rift Valley fever virus replication. Viruses 2, 731\u2013747 (2010).","journal-title":"Viruses"},{"key":"e_1_3_4_29_2","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1128\/jvi.63.1.122-128.1989","article-title":"The ends of La Crosse virus genome and antigenome RNAs within nucleocapsids are base paired","volume":"63","author":"Raju R","year":"1989","unstructured":"R Raju, D Kolakofsky, The ends of La Crosse virus genome and antigenome RNAs within nucleocapsids are base paired. J Virol 63, 122\u2013128 (1989).","journal-title":"J Virol"},{"key":"e_1_3_4_30_2","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1007\/978-1-4899-1364-7_7","volume-title":"The Bunyaviridae","author":"Pettersson RF","year":"1996","unstructured":"RF Pettersson, L Melin The Bunyaviridae, ed RM Elliott (Plenum, New York), pp. 159\u2013188 (1996)."},{"key":"e_1_3_4_31_2","doi-asserted-by":"crossref","first-page":"11381","DOI":"10.1128\/JVI.00767-07","article-title":"The cytoplasmic tails of Uukuniemi Virus (Bunyaviridae) G\n                  N and G\n                  C glycoproteins are important for intracellular targeting and the budding of virus-like particles","volume":"81","author":"Overby AK","year":"2007","unstructured":"AK Overby, VL Popov, RF Pettersson, EP Neve, The cytoplasmic tails of Uukuniemi Virus (Bunyaviridae) GN and GC glycoproteins are important for intracellular targeting and the budding of virus-like particles. J Virol 81, 11381\u201311391 (2007).","journal-title":"J Virol"},{"key":"e_1_3_4_32_2","doi-asserted-by":"crossref","first-page":"3173","DOI":"10.1099\/0022-1317-80-12-3173","article-title":"Bunyavirus superinfection and segment reassortment in transovarially infected mosquitoes","volume":"80","author":"Borucki MK","year":"1999","unstructured":"MK Borucki, LJ Chandler, BM Parker, CD Blair, BJ Beaty, Bunyavirus superinfection and segment reassortment in transovarially infected mosquitoes. J Gen Virol 80, 3173\u20133179 (1999).","journal-title":"J Gen Virol"},{"key":"e_1_3_4_33_2","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1016\/0168-1702(91)90108-8","article-title":"Reassortment of La Crosse and Tahyna bunyaviruses in Aedes triseriatus mosquitoes","volume":"20","author":"Chandler LJ","year":"1991","unstructured":"LJ Chandler, et al., Reassortment of La Crosse and Tahyna bunyaviruses in Aedes triseriatus mosquitoes. Virus Res 20, 181\u2013191 (1991).","journal-title":"Virus Res"},{"key":"e_1_3_4_34_2","doi-asserted-by":"crossref","first-page":"548","DOI":"10.1126\/science.4048949","article-title":"Evolution of bunyaviruses by genome reassortment in dually infected mosquitoes (Aedes triseriatus)","volume":"230","author":"Beaty BJ","year":"1985","unstructured":"BJ Beaty, DR Sundin, LJ Chandler, DH Bishop, Evolution of bunyaviruses by genome reassortment in dually infected mosquitoes (Aedes triseriatus). Science 230, 548\u2013550 (1985).","journal-title":"Science"},{"key":"e_1_3_4_35_2","doi-asserted-by":"crossref","first-page":"2237","DOI":"10.1007\/s00705-007-1069-z","article-title":"Natural M-segment reassortment in Potosi and Main Drain viruses: Implications for the evolution of orthobunyaviruses","volume":"152","author":"Briese T","year":"2007","unstructured":"T Briese, V Kapoor, WI Lipkin, Natural M-segment reassortment in Potosi and Main Drain viruses: Implications for the evolution of orthobunyaviruses. Arch Virol 152, 2237\u20132247 (2007).","journal-title":"Arch Virol"},{"key":"e_1_3_4_36_2","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1006\/viro.2001.1201","article-title":"A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia","volume":"291","author":"Bowen MD","year":"2001","unstructured":"MD Bowen, et al., A reassortant bunyavirus isolated from acute hemorrhagic fever cases in Kenya and Somalia. Virology 291, 185\u2013190 (2001).","journal-title":"Virology"},{"key":"e_1_3_4_37_2","doi-asserted-by":"crossref","first-page":"12200","DOI":"10.1128\/JVI.76.23.12200-12210.2002","article-title":"Characterization of the Golgi retention motif of Rift Valley fever virus G\n                  N glycoprotein","volume":"76","author":"Gerrard SR","year":"2002","unstructured":"SR Gerrard, ST Nichol, Characterization of the Golgi retention motif of Rift Valley fever virus GN glycoprotein. J Virol 76, 12200\u201312210 (2002).","journal-title":"J Virol"},{"key":"e_1_3_4_38_2","doi-asserted-by":"crossref","first-page":"1519","DOI":"10.1016\/j.str.2004.05.023","article-title":"A basis for SUMO protease specificity provided by analysis of human Senp2 and a Senp2-SUMO complex","volume":"12","author":"Reverter D","year":"2004","unstructured":"D Reverter, CD Lima, A basis for SUMO protease specificity provided by analysis of human Senp2 and a Senp2-SUMO complex. Structure 12, 1519\u20131531 (2004).","journal-title":"Structure"}],"container-title":["Proceedings of the National Academy of Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/pnas.org\/doi\/pdf\/10.1073\/pnas.1001760107","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,6,7]],"date-time":"2022-06-07T02:49:47Z","timestamp":1654570187000},"score":1,"resource":{"primary":{"URL":"https:\/\/pnas.org\/doi\/full\/10.1073\/pnas.1001760107"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2010,6,14]]},"references-count":38,"journal-issue":{"issue":"26","published-print":{"date-parts":[[2010,6,29]]}},"alternative-id":["10.1073\/pnas.1001760107"],"URL":"https:\/\/doi.org\/10.1073\/pnas.1001760107","relation":{},"ISSN":["0027-8424","1091-6490"],"issn-type":[{"value":"0027-8424","type":"print"},{"value":"1091-6490","type":"electronic"}],"subject":[],"published":{"date-parts":[[2010,6,14]]},"assertion":[{"value":"2010-06-14","order":2,"name":"published","label":"Published","group":{"name":"publication_history","label":"Publication History"}}]}}